Interpretive Summary: In many orchard replant sites, young apple trees (Malus X domestica BORKH.) develop poorly, suffering necrotic lesions of fine feeder roots, nutrient and drought stress, stunted growth, and reduced yields. This soil-borne disease syndrome is known as Apple Replant Disease (ARD), and its putative causal pathogens include soil-borne fungi, bacteria, nematodes, actinobacteria, and oomycetes, in site-specific combinations. These pathogens accumulate in the root-zone of previous fruit trees, often without causing visible harm to those established trees, but seriously damaging newly planted trees on susceptible rootstocks. Even when orchards are planted in sites with no history of fruit growing, apple root pathogens can become problematic within a few years. Modern orchards usually consist of trees propagated by grafting buds of a scion cultivar (a cultivated genotype) onto clonally propagated rootstocks that determine important tree traits such as size (vigor), yield precocity and efficiency, and adaptability to soil physical, chemical and biological conditions. These apple rootstocks are propagated from rooted vegetative cuttings in nursery layering beds, so that all rootstocks of a given cultivar represent a single mass-produced genotype. The Cornell-Geneva (CG) rootstock breeding program has emphasized selection for genotypes with multiple disease resistance and several rootstocks from the CG program are reportedly resistant or tolerant to ARD. This research identified a rootstock effect in causing a shift in the microbial community that causes ARD. Rootstocks that are reported to be tolerant or resistant to ARD may not cause ARD for subsequent plantings.

Technical Abstract:
Apple replant disease (ARD) is a soil-borne disease complex that affects young apple trees in replanted orchards, resulting in stunted growth and reduced yields. New rootstock genotypes with resistance to ARD may help to control this disease. To determine the effects of rootstock genotype successional rotations during orchard renovation, we investigated root-zone soil microbial consortia and the relative severity of ARD on seven rootstock genotypes (M.9, M.26, G.30, G.41, G.65, G.935, and CG.6210) planted in soil where trees on four of those same rootstocks (M.9, M.26, G.30 and CG.6210) had grown for the previous 15 years. The G.935 and CG.6210 rootstocks grew more vigorously in soil where CG.6210 had previously grown; G.41 grew better in soil where M.26 had previously grown, and G.30 grew better where M.9 had grown. Rootstock genotyping indicated that genetic distances among rootstocks were loosely correlated with their differential responses to ARD. Root-zone fungal and bacterial community composition, assessed by DNA fingerprinting (TRFLP), differed between M.26 and CG.6210. Soil bacterial communities were influenced mostly by the previously existing rootstock, while fungal communities were influenced more by the subsequent replant rootstock. In a clone library of bacteria from M.26 and CG.6210 root-zone soil, '-Proteobacteria was the most abundant phylum (25% of sequences). Acidobacteria were more abundant in M.26 soil (27%), than in CG.6210 soil (7%), and more Xanthomonadaceae sequences were obtained from CG.6210 soil than from M.26 soil (25% vs. 12%). Sequences representing the Burkholderia cepacia complex were obtained only from CG.6210 soil. Rootstock genotypes that had grown in the preceding orchard soil affected subsequent ARD severity, but replanting with the same or closely related rootstocks did not necessarily exacerbate this disease problem. Genotype-specific interactions with soil microbial consortia may be linked with apple rootstock tolerance or susceptibility to ARD.